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Cited by 108Advanced Neuroimaging Techniques and ApplicationsCognitive Abilities and TestingFunctional Brain Connectivity Studies

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White Matter Development in Early Puberty: A Longitudinal Volumetric and Diffusion Tensor Imaging Twin Study

Open access
Brouwer, Rachel M., Mandl, René C. W., Schnack, Hugo G., van Soelen, Inge L. C., van Baal, G. Caroline, Peper, Jiska S., Kahn, René S., Boomsma, Dorret I., Pol, H. E. Hulshoff·2012·PLoS ONE
DOI 10.1371/journal.pone.0032316PMC PMC3326005
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Abstract

White matter microstructure and volume show synchronous developmental patterns in children. White matter volume increases considerably during development. Fractional anisotropy, a measure for white matter microstructural directionality, also increases with age. Development of white matter volume and development of white matter microstructure seem to go hand in hand. The extent to which the same or different genetic and/or environmental factors drive these two aspects of white matter maturation is currently unknown. We mapped changes in white matter volume, surface area and diffusion parameters in mono- and dizygotic twins who were scanned at age 9 (203 individuals) and again at age 12 (126 individuals). Over the three-year interval, white matter volume (+6.0%) and surface area (+1.7%) increased, fiber bundles expanded (most pronounced in the left arcuate fasciculus and splenium), and fractional anisotropy increased (+3.0%). Genes influenced white matter volume (heritability ~85%), surface area (~85%), and fractional anisotropy (locally 7% to 50%) at both ages. Finally, volumetric white matter growth was negatively correlated with fractional anisotropy increase (r = -0.62) and this relationship was driven by environmental factors. In children who showed the most pronounced white matter growth, fractional anisotropy increased the least and vice-versa. Thus, white matter development in childhood may reflect a process of both expansion and fiber optimization.

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Crossref · 10.1371/journal.pone.0032316

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Figures

Figure 1 Significant tissue expansion: Significant Jacobian values > 1 overlaid on the model brain. Values range from 1.02 (purple) to 1.30 (bright red). Expansion was observed in regions covering the arcuate fasciculus (E), cerebellar penduncle (A), cinguli (C) , corpus callosum (B,C), cortical spinal tract (B,F), uncinate fasciculus (D) and on the gray matter / cerebral spinal fluid boundary (A-F), the latter likely representing brain growth. For visualization purposes, values were resampled to model brain resolution.
Figure 1 Significant tissue expansion: Significant Jacobian values > 1 overlaid on the model brain. Values range from 1.02 (purple) to 1.30 (bright red). Expansion was observed in regions covering the arcuate fasciculus (E), cerebellar penduncle (A), cinguli (C) , corpus callosum (B,C), cortical spinal tract (B,F), uncinate fasciculus (D) and on the gray matter / cerebral spinal fluid boundary (A-F), the latter likely representing brain growth. For visualization purposes, values were resampled to model brain resolution.CC BY · PubMed Central
Figure 2 Increases of relative fractional anisotropy between the ages of 9 and 12, projected onto the group average fiber bundle. Left, top and right view. For visualization purposes, values were smoothed along the bundle using LOESS [59].
Figure 2 Increases of relative fractional anisotropy between the ages of 9 and 12, projected onto the group average fiber bundle. Left, top and right view. For visualization purposes, values were smoothed along the bundle using LOESS [59].CC BY · PubMed Central
Figure 3 The relationship between changes in pure white matter fractional anisotropy and changes in white matter volume in the three-year interval.
Figure 3 The relationship between changes in pure white matter fractional anisotropy and changes in white matter volume in the three-year interval.CC BY · PubMed Central
Figure 4 Relative white matter surface area expansion of AAL regions in the left and right hemisphere. Please note that expansion is based (and projected on) AAL regions rather than representing continuous expansion. *Areas in which girls had larger expansion than boys.
Figure 4 Relative white matter surface area expansion of AAL regions in the left and right hemisphere. Please note that expansion is based (and projected on) AAL regions rather than representing continuous expansion. *Areas in which girls had larger expansion than boys.CC BY · PubMed Central
Figure 5 Histograms of fractional anisotropy in pure white matter at age 9 and age 12. In the 14 children with relatively large volumetric white matter growth mean fractional anisotropy was 0.43 at both ages. In 13 children with relatively small volumetric white matter growth, mean fractional anisotropy increased from 0.41 to 0.44.
Figure 5 Histograms of fractional anisotropy in pure white matter at age 9 and age 12. In the 14 children with relatively large volumetric white matter growth mean fractional anisotropy was 0.43 at both ages. In 13 children with relatively small volumetric white matter growth, mean fractional anisotropy increased from 0.41 to 0.44.CC BY · PubMed Central

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Citations

Cites

Research works printed but not linked: 2

  1. ILC van Soelen, 2011, Heritability of volumetric changes during brain development., Hum Brain Map, Dec, 3
  2. MC Neale, 2006, 'Mx: statistical modeling', VCU Box 900126, Richmond, VA 23298: Department of Psychiatry, 7th Edition

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Metadata

Authors
Brouwer, R. M., Mandl, R. C. W., Schnack, H. G., van Soelen, I. L. C., van Baal, G. C., Peper, J. S., Kahn, R. S., Boomsma, D. I., & Pol, H. E. H.
Affiliations
  • University Medical Center Utrecht (NL)
  • Leiden University (NL)
  • Vrije Universiteit Amsterdam (NL)
Corresponding author
Brouwer, Rachel M.
ORCID
Venue
PLoS ONE
Publisher
Public Library of Science (PLoS)
Published
2012-04-13
Volume
7
Issue
4
Pages
e32316
ISSN
1932-6203 (ISSN-L)
DOI
10.1371/journal.pone.0032316
PMC
PMC3326005
OpenAlex
W2137931201
Cited by
107
References
62
Citations by year
2026: 2 · 2025: 4 · 2024: 2 · 2023: 6 · 2022: 8 · 2021: 9 · 2020: 12 · 2019: 5 · 2018: 8 · 2017: 10 · 2016: 10 · 2015: 13 · 2014: 9 · 2013: 8 · 2012: 1
FWCI
7.49
Type
journal article
Language
en
Open access
Licence
Locations
  • PLoS ONE (publishedVersion, cc-by)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • VU Research Portal (publishedVersion, other-oa)
  • Data Archiving and Networked Services (DANS) (submittedVersion, other-oa)
  • Leiden Repository (Leiden University) (submittedVersion)
  • Digital Academic REpository of VU University Amsterdam (Vrije Universiteit Amsterdam) (submittedVersion, cc-by)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • Data Archiving and Networked Services (DANS) (submittedVersion, cc-by)
Funders
  • Nederlandse Organisatie voor Wetenschappelijk Onderzoek (NWO 51.02.060, NWO 480-04-004, 230374, 480-04-004, 51.02.060)
  • Hersenstichting
Topics
  • Health Sciences › Medicine › Radiology, Nuclear Medicine and Imaging › Advanced Neuroimaging Techniques and Applications
  • Social Sciences › Psychology › Experimental and Cognitive Psychology › Cognitive Abilities and Testing
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Functional Brain Connectivity Studies
Keywords
white matter development, precocious puberty, fractional anisotropy, white matter volume, heritability, monozygotic twins, dizygotic twins, arcuate fasciculus, splenium, child neurodevelopment, genetic and environmental factors
MeSH terms
Brain, Child, Female, Humans, Male, Anisotropy, Diffusion Tensor Imaging

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